Prevalence of dental caries, periodontal disease, malocclusion, and tooth wear in indigenous populations in Brazil: a systematic review and meta-analysis

Abstract The aim of this review was to evaluate the prevalence of dental caries, periodontal disease, malocclusion, and tooth wear in indigenous in Brazil. A systematic review of observational studies was performed according to the PRISMA guidelines (CRD42020218704). The search strategy involved the electronic databases of Embase, LILACS, PubMed, Web of Science, Scopus, and the CAPES Theses and Dissertations for gray literature. The eligibility criteria consisted of publications that assessed the prevalence of oral conditions in indigenous populations in Brazil. Studies with indigenous people living in urban area were excluded. The risk of bias was evaluated by using JBI Critical Appraisal for prevalence studies. Thirty studies were included in the review, and the majority showed a low risk of bias. A meta-analysis of 20 studies was conducted using the random-effects model and a 95% confidence interval. Several ethnicities were studied in isolation or in groups (n = 7,627 for dental caries; n = 2,774 for periodontal disease; n = 1,067 for malocclusion; n = 150 for tooth wear). The prevalence of caries ranged from 50% among indigenous people aged 18-36 months to 100% among those aged 65–74 years. The prevalence of periodontal disease ranged from 58% to 83%. The prevalence of malocclusion was 43%. Tooth wear was assessed in only one ethnic group and showed a prevalence of 100% in indigenous people aged >18 years. The certainty of evidence assessed by the GRADE system ranged from very low to moderate. This systematic review showed significant differences in the prevalence of dental caries, periodontal disease and malocclusion between indigenous population groups and territories in which indigenous people live.


Introduction
Over half of all indigenous groups in Latin America and the Caribbean live in Brazil.These groups consist of 305 different ethnicities and speak 274 native languages, 1 which makes the Brazilian indigenous population the most ethnically diverse in the world.According to the Brazilian Health Information System for Indigenous Peoples (SIASI -Sistema de Informação da Atenção à Saúde Indígena) of the Special Secretariat for Indigenous Health (SESAI -Secretaria Especial de Saúde Indígena), there are a total of 738,624 indigenous people in 5,361 villages throughout the national territory.
Recognition of and respect for indigenous socio-diversity in Brazil was guaranteed by the Federal Constitution in 1988.This allowed the development of specific healthcare policies to meet the sociocultural and geographical peculiarities of each ethnicity and led to the approval of the Arouca Bill in 1999 (Law No. 9,836) 2 and the establishment of the Indigenous Healthcare Subsystem as part of the National Healthcare System (SUS -Sistema Único de Saúde).The healthcare model was organized by creating 34 Special Indigenous Health Districts (DSEI -Distrito Sanitário Especial Indígena) throughout the national territory.The DSEI is a dynamic ethnocultural space, and well-defined area in terms of geographic, population and administrative levels. 3he National Oral Health Policy (PNSB -Política Nacional de Saúde Bucal) emphasized the importance of knowing the epidemiological profile and oral health problems of different indigenous groups, not only in terms of the most prevalent diseases, but also their socioeconomic conditions, habits, lifestyles and health needs, for better planning of public policies. 4The contact of nonindigenous population with the indigenous people has brought about changes in their subsistence, resulting in a negative impact on the oral health of these individuals. 5,6ecent studies on this topic only report general data from South America.In a systematic review on dental caries in indigenous people, the authors showed that caries was a public health problem for these people and prevention and treatment strategies must consider cultural specificities. 7Based on this review, the levels of dental caries among indigenous people are high when compared with those of the general population of Brazil, Chile, Uruguay, and Venezuela in all age groups. 8urthermore, it has recently been shown that irrespective of age, sex or country, the worldwide prevalence and severity of dental caries are higher among indigenous groups when compared with nonindigenous groups and this is particularly noticeable in untreated dental caries and tooth loss. 9Reducing these inequalities in indigenous oral health at a global level initially involves a solid understanding of the magnitude of inequalities that indigenous populations continue to experience. 10 Dental caries followed by periodontal disease has been the most frequently oral disease addressed in these populations due to its relevance from the public health point of view, with recognized impacts on the quality of life of affected individuals. 11Whereas despite some important local studies that have been conducted with indigenous groups, other problems such as malocclusion 5,[12][13][14][15] and tooth wear 16 have not yet been extensively studied.
The sociocultural diversity of Brazilian indigenous people, their living and health conditions reinforce the need to disseminate knowledge of different epidemiological profiles and health surveillance actions that address the specificities of different indigenous ethnicities.Systematic reviews offer a high level of evidence, and the results can help guide and assess public health policies.Thus, the objective of this review was to summarize the available data on the prevalence of oral diseases and conditions, such as dental caries, periodontal disease, malocclusion, and tooth wear in indigenous people in Brazil and thus contribute to understanding the burden of these conditions on these populations.

Methodology Protocol and registration
This systematic review was performed following the JBI Manual for Evidence Synthesis 17 and reported in accordance with the Preferred Reporting Items Checklist for Systematic Reviews and Meta-Analyses (PRISMA Statement). 18A protocol was registered at the International Prospective Registry of Systematic Reviews (PROSPERO) database under number CRD42020218704.

Eligibility criteria
The inclusion criteria were defined according to the CoCoPop strategy (Condition, Context, carried out independently by two authors (JMRV and JVP) and disagreements were resolved by a third researcher from the team (MABR).

Risk of bias assessment
The Joan na Briggs Institute (JBI) Critical Appraisal Tool for Prevalence Studies 20 was used to assess the risk of bias of the studies included.The analysis was performed independently by two authors (JMRV and JVP) and disagreements were assessed by a third author (MABR).The reviewers scored each item with "yes", "no", "unclear" and "not applicable".Studies were categorized as: a) low risk of bias, if studies attained over 70% of "yes" scores; b) moderate risk of bias, if "yes" scores were between 50% and 69%; and c) high risk of bias, if "yes" scores were below 49% 21 .

Effect measures
The primary outcome was the prevalence of oral conditions including dental caries, periodontal disease, malocclusion, and tooth wear.The measure of effect used was the event rate and confidence interval for each of the conditions studied.

Certainty assessment
Certainty of the evidence identified was assessed by the Grading of Recommendation, Assessment, Development, and Evaluation (GRADE) tool. 27In the absence of a formal procedure for the assessment of certainty in prevalence estimates, we applied the framework developed for the incidence estimates in the context of prognostic studies. 28For the meta-analysis of prevalence, the best evidence is obtained through cross-sectional studies or baseline examination from cohort studies.Thus, the assessment of evidence from these types of studies begins with a "high certainty of evidence", and is downgraded depending on the risk of bias, inconsistency, indirectness, imprecision, and publication bias.Finally, the level of certainty among the items of evidence identified can be characterized as high, moderate, low, or very low.

Study selection
The search in the databases resulted in 1,566 articles.After removing duplicates, 1,066 studies were read for titles and abstracts, and 47 were selected for a full reading.2][43][44][45][46][47][48][49][50][51][52] Some of these studies addressed more than one clinical condition.The studies excluded and the reasons for exclusion are shown in Table 2.

Malocclusion
The prevalence of malocclusion in indigenous people in Brazil was reported in 7 studies (Table 5).Of these studies, two were published in the 60s and 70s, 14,16 three from 2000 to 2007 4,13,42 and two between 2011 and 2015. 12,15mong the various ethnic groups in the Brazilian territory, the studies included the Xavante, 5,14 Bakairi, 14 Yanomami, 16 Guarani-Mbya, 42 Enawenê-Nawê, 13 Arara-Laranjal, Arara-Iriri, 15 Asurini, Pat-Krô, Pikayaka. 12he ethnicities studied totaled 1,067 indigenous people.Only one study was unclear about the number of individuals being screened.Relative to the division by sex (male/female), only one study reported this number. 5The studies were carried out in the states of Mato Grosso, 5,13,14 Pará, 12,15 Roraima, 16 and São Paulo. 42e malocclusion condition was assessed by the Angle Classification 5,12,14 and Dental Aesthetic Index -DAI. 42One study 15 used the Björk method, 53 one other study used the classification of the National Institute of Dental Research -NIDR, 16 and another study did not inform the index/instrument used. 13

Tooth wear
Tooth wear was assessed in one study. 16The ethnic group studied was the Yanomami, who live in the state of Roraima, totaling 150 (79 male and 71 female) indigenous individuals, aged between 13 and 18 years and adults over the age of 18 years.The instrument used was the Pedersen index for cervical abrasion and the Broca index for occlusal wear (Table 6).
The only study that assessed tooth wear presented a high risk of bias due to sampling, lack of standardization for measurement conditions and data analysis.In addition, the study did not clearly state all the conditions assessed. 16The risk of bias assessment is shown in Table 7.

Results of individual studies and syntheses
The results of the individual studies are presented in Tables 3-6.Synthesis of the results is presented by oral health condition assessed.

Dental caries
The meta-analysis of the prevalence of dental caries in the indigenous population aged 18-36 months included three studies 36,44,48 and presented an effect estimate of 50% (95%CI: 31-69, I² = 87%).Sensitivity testing for this analysis was not performed as no outliers were detected (Figure 2A).

Certainty of evidence
The GRADE approach was used to assess eighteen outcomes.Two analyses of caries prevalence (age group 5 years and 15 to 19 years) were classified as moderate level of certainty.All other analyses were categorized as low or very low level of certainty, which means the true effect may be substantially different from the estimate of the effect.Table 8 shows more details for each outcome assessed.

Discussion
The present review analyzed the prevalence of dental caries, periodontal disease, malocclusion, and tooth wear in indigenous people of Brazil living in indigenous lands.The study differs from other published reviews in that it assessed all age groups and addressed the above-mentioned conditions together.Thus it revealed an important variation in the prevalence of these conditions among different indigenous people.It is worth mentioning that these differences were also found within the same geographic region, and in the same ethnic group inhabiting different regions.
The prevalence of dental caries in the population aged 18-36 months was 37% in the Kaiabi, Yudjá, Ikpeng, Trumai, Kamaiurá, Waurá, Kisedjê, Panará and Tapaiuna ethnic groups in the Xingú Indigenous Park-MT and 70% in the Parakanã ethnic group in the state of Pará.The high heterogeneity observed in the meta-analysis can be explained by geographic differences (North, Northeast, and Midwest regions) and by the sociocultural diversity of the different ethnicities studied.The summary prevalence of dental caries (50%) in the indigenous population   54 The highest prevalence found (70%) was for the Parakanã ethnic group, which can be attributed to the history of contact with urban population and important milestones such as the construction of the Tocantins railroad in the 1920s, the Transamazon highway in the 70s, and the Tucuruí hydroelectric power station in the 1980s that began operating in 1984. 48These changes impacted the dynamics of the health-disease process of this population.Health care was focused on assisting the individuals affected by the diseases that plagued these indigenous people, but no health promotion and disease prevention  Prevalence of dental caries, periodontal disease, malocclusion, and tooth wear in indigenous populations in Brazil: a systematic review and meta-analysis actions were developed.Relative to oral health, the same reasoning was followed, and care was focused on tooth extractions that were sporadically performed, and oral health care actions lacked a systematization. 48,55

Very low
a Very serious inconsistency.Substantial heterogeneity (I 2 > 50%) and point estimates and confidence intervals vary considerably; b The sample of the studies included were from specific populations; c Very serious imprecision.The confidence interval of the effect estimate varied by over 10%; d Publication bias not assessed due to low number of studies (< 10); e Serious imprecision.The confidence interval of the effect estimate varied by over 5%, but less than 10%; f Serious inconsistency.Substantial heterogeneity (I 2 > 50%), but there was overlap of the confidence intervals; g Half of the eligible studies were at high risk of bias.
4][65] Periodontal disease in indigenous people has hardly been studied and the studies included in the qualitative analysis were heterogeneous in terms of method, instruments used, analysis by sextants or total arches, and the conditions of gingival bleeding, dental calculus, and periodontal pockets were reported globally or individually.
The prevalence of periodontal disease observed in the present study showed a significant difference between studies, considering ethnic groupings or a particular ethnicity.This result suggested that in addition to the accumulation of biofilm, periodontal diseases are influenced by sociocultural and environmental factors.In this context, socioeconomic status and plaque index > 40% was associated with the indication of tooth extraction in the Kiriri ethnic group 66 .In the population aged 15-19 years and 35-44 years, the lowest prevalence (32% and 38%, respectively) was observed in the Guarani who live in villages on the coast of São Paulo and Rio de Janeiro. 39Access to the villages occurs by land and sea, which has favored the development of health promotion activities and oral health care since 1993.In the Yanomami of the Xitei-Ketaa-RR Pole, 43 the prevalence observed was above 90% in all age groups studied.This could be attributed to the predominantly pasty, less abrasive diet, favoring the biofilm accumulation and consequent gingival inflammation.In the lower and middle Xingu ethnic groups, the prevalence ranged from 55% in the elderly population to 92% in the 35-44 age group, higher than that found in the nonindigenous population. 54It is worth mentioning that the adult and elderly had a considerable number of sextants excluded due to edentulism, 47 as observed in the Enawenê-Nawê ethnic group. 13A recent systematic review showed that the prevalence of periodontitis was 35% (95%CI: 0.18-0.52)higher among the indigenous population than the nonindigenous population. 67he prevalence of gingival bleeding in adolescents (27%) was lower than the national average for the urban population (33.8%). 57However, it would be important to highlight that the prevalence found in the Yanomami inhabitants of the Polo Base Xitei-Ketaa-RR was the highest, 62%, and this was also observed in the urban population of the northern region (51.0%). 57Dental calculus was more prevalent (52%) in the population aged 35-44 years, but with indices lower than those found in the urban population (64.1%). 57alocclusion in indigenous people has not been widely studied and the studies included in the qualitative analysis, which assessed malocclusion, were heterogeneous in terms of the age groups and methodology.The prevalence found in the present study ranged from 14% to 86% with a mean of 43% in the quantitative analysis, considering all age groups analyzed.The data found were lower than those found for the world average (56%) and the Americas (53%) 68 and higher than the national average in urban population (37.6% and 36.0% in the age group 12 and 15-19 years, respectively). 57Malocclusion in indigenous Brazilians has been associated with genetic factors that substantially contribute to the morphology of occlusal and facial features in the indigenous groups studied, as observed in the Arara-laranjal, Arara-iriri 15 and Asurini, Pat-krô and Pikayaká 12 ethnicities.The study carried out in the 1970s, which assessed malocclusion in the Yanomami population, concluded that the influence of mastication on the evolution of human dentition did not appear to be preponderant; physiological occlusal wear eliminated dental cusps, but this did not decrease masticatory efficiency; occlusal interferences caused attrition asymmetry; and physiological proximal wear had little influence on anterior crowding. 16Therefore, the prevalence of malocclusion in indigenous populations must be assessed in other ethnic groups, and so must the changes that have occurred in sociocultural aspects.
In relation to tooth wear, the only study included showed a high prevalence in the Yanomami ethnicity (64.3% at 13-18 years old and 100% in those over 18 years old). 16In turn, the results of a recent study on the Macuxi ethnic group (Roraima, Brazil) showed a prevalence of tooth wear of 38.1% and that indigenous adults have a greater chance of tooth wear (8.09CI 3. 70-17.98)than adolescents. 69The prevalence of tooth wear in population-based studies in permanent teeth of children and adolescents was reported by Braz.Oral Res.2023:37:e094 Prevalence of dental caries, periodontal disease, malocclusion, and tooth wear in indigenous populations in Brazil: a systematic review and meta-analysis a systematic review and indicated a prevalence of 30.4%, however, with high heterogeneity between studies.According to the authors, the correct choice of a clinical index for detecting dental erosion and the geographic location play an important role in the great variability of erosive tooth wear in permanent teeth of children and adolescents. 70he strength of the present review was that the study did not include self-declared indigenous individuals living in urban areas, but only included individuals living in indigenous territory.This approach was in line with the aspects pointed out in the literature, which considered it a challenge to have consistent data on the indigenous population due to the way people self-identify. 71n the other hand, the results should be interpreted with attention considering that the quality of the studies included may have affected the results of this systematic review.The main limitation of this systematic review and meta-analysis was the low certainty of the body of evidence, which was justified by the high heterogeneity of estimates; indirect evidence, as the samples of the studies included in the analysis were from specific indigenous ethnicities and not representative of the entire indigenous population in Brazil.A further limitation was the imprecision of the data due to the great variation in the confidence intervals of the analyses.Furthermore, it was not possible to analyze and compare ethnicities in isolation, as many studies analyzed several ethnicities, and presented a single result in a grouped form.
New approaches with representative samples of ethnicities and with standardized dental disease outcomes 71 in alignment with population-based studies need to be carried out, as well as analysis within the context of the life of these populations.Based on our results, a nationwide survey on the oral health conditions of the different indigenous people in Brazil must be conducted as it would substantially contribute to the development of strategies for action and organization of health services in accordance with the different realities of each Special Indigenous Health District (DSEI).

Conclusion
Based on limited evidence, this study reported significant differences in prevalence of dental caries, periodontal disease, and malocclusion in the Brazilian indigenous population.These variations resulted from the great diversity among Brazilian indigenous people; that is, different socioeconomic, environmental, and cultural conditions.Furthermore, the instruments used, and the results reported need to be standardized and improved in future research involving indigenous people.

Figure 1 .( 2 )
Figure 1.Flow diagram of literature search and selection criteria.

Figure 2 .
Figure 2. Forest plot of dental caries: A: Prevalence in the indigenous population aged 18-36 months; B: Prevalence of dental caries in the 5-year-old indigenous population; C: Sensitivity analysis after removal of outlier values of dental caries prevalence in the 5-year-old indigenous population; D: Prevalence of dental caries in the 12-year-old indigenous population; E: Sensitivity analysis after removal of outlier values of dental caries prevalence in a 12-year-old indigenous population.

Figure 3 .
Figure 3. Forest plot of dental caries: A: Prevalence of dental caries in the indigenous population aged 15-19 years; B: Sensitivity analysis after removal of outlier values of dental caries prevalence in the indigenous population aged 15-19 years; C: Prevalence of dental caries in the indigenous population aged 35-44 years; D: Prevalence of dental caries in the indigenous population aged 65-74 years.

Figure 4 .
Figure 4. Forest plot of periodontal disease: A: Prevalence of periodontal disease in the indigenous population aged 15-19 years; B: Prevalence of periodontal disease in the indigenous population aged 35-44 years; C: Prevalence of periodontal disease in the indigenous population aged 65-74 years; D: Sensitivity analysis after removal of outlier values of the prevalence of periodontal disease in the indigenous population aged 65-74 years.

Figure 5 .
Figure 5. Forest plot of gingival bleeding: A: Prevalence of gingival bleeding in the indigenous population aged 15-19 years; B: Prevalence of gingival bleeding in the indigenous population aged 35-44 years; C: Prevalence of gingival bleeding in the indigenous population aged 65-74 years.

Figure 6 .
Figure 6.Forest plot of dental calculus: A: Prevalence of dental calculus in the indigenous population aged 15-19 years; B: Prevalence of dental calculus in the indigenous population aged 35-44 years; C: Prevalence of dental calculus in the indigenous population aged 65-74 years; D: Sensitivity analysis after outlier removal of dental calculus prevalence in the indigenous population aged 65-74 years.

Figure 7 .
Figure 7. Forest plot of periodontal pocket: A: Prevalence of periodontal pockets in the indigenous population aged 35-44 years; B: Prevalence of periodontal pockets in the indigenous population aged 65-74 years.

Figure 8 .
Figure 8. A: Forest plot of prevalence of malocclusion in the indigenous population; B: Sensitivity analysis after removal of outlier values of malocclusion prevalence in the indigenous population.

Table 3 .
Description of included studies for dental caries.

Table 4 .
Description of included studies for Periodontal disease.
Braz.Oral Res.2023:37:e094Prevalence of dental caries, periodontal disease, malocclusion, and tooth wear in indigenous populations in Brazil: a systematic review and meta-analysis

Table 5 .
Description of included studies for malocclusion.

Table 6 .
Description of included studies for tooth wear condition.

Table 7 .
Risk of Bias assessed by the Joanna Briggs Institute Critical Appraisal checklist for prevalence studies for use in JBI Systematic Reviews.Risk of bias was categorized as High when the study reaches up to 49% score "yes", Moderate when the study reached 50% to 69% score "yes", and Low when the study reached more than 70% score "yes".
Was the sample size adequate?Q4.Were the study subjects and the setting described in detail?Q5.Was the data analysis conducted with sufficient coverage of the identified sample?Q6 Were valid methods used for the identification of the condition?Q7.Was the condition measured in a standard, reliable way for all participants?Q8.Was there appropriate statistical analysis?Q9.Was the response rate adequate, and if not, was the low response rate managed appropriately?Y:-Yes; N: No; U: Unclear, NA: Not applicable; H: High, M: Moderate; L:-Low.

Table 8 .
Grading of Recommendations Assessment, Development, and Evaluation (GRADE) Summary of Findings Table for the Outcomes of the Systematic Review and Meta-Analysis.